Abstract
The present study was carried out to evaluate the genotoxic potential of nutritional quality of feed, using erythrocytic nuclear abnormalities assay in Nile tilapia and its correlation with available nutrients and common fish growth biomarkers. For this, ten feeds commercialized in Brazil were assessed on digestibility and performance assays with triplicate groups. Venipuncture of the caudal vein for abnormalities analyzed was performed 102 days after the fish were fed with the commercial feed twice a day, to apparent satiation. Nuclear abnormalities were analyzed in blood smears. Principal component analysis and correlation matrix were used to carry out an exploratory analysis of correlation between frequency of abnormalities and performance parameters or available nutrients. The frequency of abnormalities in erythrocytes of Nile tilapia, fish performance, and digestibility were feed-dependent. It was observed correlations between the frequency of most abnormalities and performance parameters or content of nutrients. The frequency of kidney-shaped (6.23 ± 4.14), bud nuclei (2.99 ± 1.95), bridge nuclei (0.53 ± 0.50), and binuclei (0.43 ± 0.59) was the highest in fish that also presented the worst performance among all treatments and correlated with digestible methionine. Micronucleus frequency (0.33 ± 0.49) was higher in fish from the same group that presented depressed feed intake and lower available zinc. Only one group presented vacuolated nuclei and the frequency of this abnormality was correlated with available phosphorus. The frequency of abnormalities in erythrocytes is a fish sensitive indicator of health and plays an important role as a complementary tool in the assessment of fish feeding. The variation in the frequency of nuclear abnormalities in erythrocytes obtained among fish fed with the different feeds allows the assertion that they contained genotoxic factors.
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References
Adhikari S, Sarkar B (2004) Effect of cypermethrin and carbofuran on certain haematological parameters and prediction of their recovery in a freshwater teleost Labeo rohita (Ham.). Ecotoxicol Environ Saf 58:220–226. https://doi.org/10.1016/j.ecoenv.2003.12.003
Aissa AF, Gomes TDUH, Almeida MR, Hernandes LC, Darin JDC, Bianchi MLP, Antunes LMG (2013) Methionine concentration in the diet has a tissue-specific effect on chromosomal stability in female mice. Food Chem Toxicol 62:456–462. https://doi.org/10.1016/j.fct.2013.09.004
Alkaladi A, El-Deen NAMN, Osama MA, Zinadah AA (2015) Hematological and biochemical investigations on the effect of vitamin E and C on Oreochromis niloticus exposed to zinc oxide nanoparticles. Saudi J Biol Sci 22:556–563. https://doi.org/10.1016/j.sjbs.2015.02.012
AOAC (2012) The official methods of analysis, 19th edn Association of Official Agricultural Chemists International (AOAC), Gaithersburg, MD, USA
APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association (APHA), Washington, D.C. (Method 4500-N C. Persulfate Method)
Bender DA (2003) Nutritional biochemistry of the vitamins, 2nd edn. Cambridge University Press, Cambridge, USA
Binz RL, Sadhukhan R, Miousse IR, Garg S, Koturbash I, Zhou D, Hauer-Jensen M, Pathak R (2021) Dietary methionine deficiency enhances genetic instability in murine immune cells. Int J Mol Sci 22:2378–2390. https://doi.org/10.3390/ijms22052378
Bolognesi C, Hayashi M (2011) Micronucleus Assay in Aquatic Animals. Mutagen 26(1):205–213. https://doi.org/10.1093/mutage/geq073
Boonanuntanasarn S, Jangprai A, Kumkhong S, Plagnes-Juan E, Veron V, Burel C, Marandel L, Panserat S (2018) Adaptation of Nile tilapia (Oreochromis niloticus) to different levels of dietary carbohydrates: new insights from a long term nutritional study. Aquaculture 496:58–65. https://doi.org/10.1016/j.aquaculture.2018.07.011
Braham RP, Blazer VS, Shaw CH, Mazik PM (2017) Micronuclei and other erythrocyte nuclear abnormalities in fishes from the Great Lakes Basin, USA. Environ Mol Mutagen 58:570–581. https://doi.org/10.1002/em.22123
Cavaş T, Garanko NN, Arkhipchuk VV (2005) Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem Toxicol 43:569–574. https://doi.org/10.1016/j.fct.2004.12.014
Cho CY, Cowey CB, Watanabe T (1985) Finfish nutrition in Asia: methodological approaches to research and development. Ottawa, Ont., IDRC
Coutinho F, Simões R, Monge-Ortiz R, Furuya WM, Pousão-Ferreira P, Kaushik S, Oliva-Teles A, Peres H (2017) Effects of dietary methionine and taurine supplementation to low fish meal diets on growth performance and oxidative status of European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 479:447–454. https://doi.org/10.1016/j.aquaculture.2017.06.017
Dabrowska H, Meyer-Burgdorff K, Günther K-D (1989) Interaction between dietary protein and magnesium level in tilapia (Oreochromis niloticus). Aquaculture 76:277–291. https://doi.org/10.1016/0044-8486(89)90081-1
Dreosti IE (2001) Zinc and the Gene. Mut Res 475:161–167. https://doi.org/10.1016/S0027-5107(01)00067-7
El-Serafy SS, Zowail ME, Abdel-Hameid N-AH, Awwad MH, Nafie EHO (2015) High dietborne Cu and Cd induced genotoxicity of Nile tilapia (Oreochromis niloticus). Environ Toxicol Pharmacol 39:1139–1147. https://doi.org/10.1016/j.etap.2015.04.001
Fenech M (2020) The Role of Nutrition in DNA Replication, DNA Damage Prevention and DNA Repair. In: De Caterina R, Martinez JA, Kohlmeier M (eds) Principles of Nutrigenetics and Nutrigenomics. Academic Press, London, pp 27–32
Feng L, Tan L-N, Liu Y, Jiang WD, Hu K, Li S-H, Zhou X-Q (2011) Influence of dietary zinc on lipid peroxidation, protein oxidation and antioxidant defence of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 17:e875–e882. https://doi.org/10.1111/j.1365-2095.2011.00858.x
Fernandes Junior AC, Carvalho PLPF, Pezzato LE, Koch JFA, Teixeira CP, Cintra FT, Damasceno FM, Amorin RL, Padovani CR, Barros MM (2016) The effect of digestible protein to digestible energy ratio and choline supplementation on growth, hematological parameters, liver steatosis and size-sorting stress response in Nile tilapia under field condition. Aquaculture 456:83–93. https://doi.org/10.1016/j.aquaculture.2016.02.001
Fracalossi DM, Rodrigues APO, Silva TSC, Cyrino JEP (2012) Técnicas experimentais em nutrição de peixes. In: Fracalossi DM, Cyrino JEP (eds) Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira. Sociedade Brasileira de Aquicultura e Biologia Aquática (in Portuguese), Florianópolis, pp 37–63
Fraker PJ, King LE, Laakko T, Vollmer TL (2000) The dynamic link between the integrity of the immune system and zinc status. J Nutr 130:1399S-1406S. https://doi.org/10.1093/jn/130.5.13
Friendly M (2002) Corrgrams: exploratory displays for correlation matrices. Am Stat 56:316–324. https://doi.org/10.1198/000313002533
Furuya WM (2010) Tabelas brasileiras para a nutrição de tilápias. GFM (in Portuguese), Toledo
Furuya WM, Pezzato LE, Barros MM, Cyrino JEP (2012) Exigências nutricionais e alimentação da tilápia. In: Fracalossi DM, Cyrino JEP (eds) Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira. Sociedade Brasileira de Aquicultura e Biologia Aquática (in Portuguese), Florianópolis, pp 255–268
Glencross BD, Baily J, Berntssen MHG, Hardy R, MacKenzie S, Tocher DR (2019) Risk assessment of the use of alternative animal and plant raw material resources in aquaculture feeds. Rev Aquaculture 12:753–758. https://onlinelibrary.wiley.com/doi/pdf/10.1111/raq.12347
Gross A, Boyd CE (1998) A digestion procedure for the simultaneous determination of total nitrogen and total phosphorus in pond water. J World Aquac Soc 29:300–303. https://doi.org/10.1111/j.1749-7345.1998.tb00650.x
Harabawy ASA, Mosleh YYI (2014) The role of vitamins A, C, E and selenium as antioxidants against genotoxicity and cytotoxicity of cadmium, copper, lead and zinc on erythrocytes of Nile tilapia, Oreochromis niloticus. Ecotoxicol Environ Saf 104:28–35. https://doi.org/10.1016/j.ecoenv.2014.02.015
Hardy RW (2001) Nutritional deficiencies in commercial aquaculture: likelihood, onset, and identification. In: Lim C, Webster CD (eds) Nutrition and fish health. CRC Press, London, NY, pp 131–148
Hashimoto EH, Kamogae M, Vanzella TP, Cólus IMS, Bracarense APFRL, Bittencourt-Oliveira MC, Itano E, Kuroda EK, Kato H, Nagata S, Ueno Y, Harada K-I, Hirooka EY (2012) Biomonitoring of microcystin and aflatoxin co-occurrence in aquaculture using immunohistochemistry and genotoxicity assays. Braz Arch Biol Technol 55(1):151–159. https://pesquisa.bvsalud.org/portal/resource/pt/lil-622693
Hassaan MS, Soltan MA, Agouz HM, Badr AM (2013) Influences of calcium/phosphorus ratio on supplemental microbial phytase efficiency for Nile tilapia (Oreochromis niloticus). Egypt J Aquat Res 39:205–213. https://doi.org/10.1016/j.ejar.2013.09.001
Heddle JA, Cimino MC, Hayashi M, Romagna F, Shelby MD, Tucker JD, Vanparys P, MacGregor JT (1991) Micronuclei as an index of cytogenetic damage: past, present, and future. Environ Mol Mutagen 18(4):277–291. https://doi.org/10.1002/em.2850180414
Heddle JA, Hite M, Kirkhart B, Mavournin K, Mac Gregor JT, Newell GW, Salmone MF (1993) The induction of micronuclei as a measure of genotoxicity: a report of the U.S. environmental protection agency Gene-Tox program. Mut Res 123:31–118. https://doi.org/10.1016/0165-1110(83)90047-7
Islam SM, Khan MM, Moniruzzaman M, Mostakim GM, Rahman MK (2019) Recuperation patterns in fish with reference to recovery of erythrocytes in Barbonymus gonionotus disordered by an organophosphate. Int J Environ Sci Technol 16:7535–7544. https://doi.org/10.1007/s13762-019-02425-0
Kan Y, Cengiz EI, Ugurlu P, Yanard M (2012) The protective role of vitamin E on gill and liver tissue histopathology and micronucleus frequencies in peripheral erythrocytes of Oreochromis niloticus exposed to deltamethrin. Environ Toxicol Pharmacol 34:170–179. https://doi.org/10.1016/j.etap.2012.03.009
Kawasaki I, Suzuki Y, Yanagisawa H (2013) Zinc deficiency enhances the induction of micronuclei and 8-hydroxy-2′-deoxyguanosine via superoxide radical in bone marrow of zinc-deficient rat. Biol Trace Elem Res 154:120–126. https://doi.org/10.1007/s12011-013-9706-8
Liu Q, Ye H, Xu M, Mai K, Sun Z, Tan X, Zou C, Chen S, Su N, Zhou Y, Chen L, Ye C (2020) The effect and mechanism of dietary monocalcium phosphate restriction on hepatic lipid deposition and immune status in obscure puffer. Takifugu Obscurus Aquac 524:735261. https://doi.org/10.1016/j.aquaculture.2020.735261
Lovell T (1998) Nutrition and feeding of fish. Springer Science + Business Media, New York
Maas RM, Verdegem MCJ, Schrama JW (2019) Effect of non-starch polysaccharide composition and enzyme supplementation on growth performance and nutrient digestibility in Nile tilapia (Oreochromis niloticus). Aquac Nutr 25:622–632. https://doi.org/10.1111/anu.12884
Michelato M, Zaminhan M, Boscolo WR, Nogaroto V, Vicari M, Artoni RF, Furuya VRB, Furuya WM (2017) Dietary histidine requirement of Nile tilapia juveniles based on growth performance, expression of muscle-growth-related genes and haematological responses. Aquaculture 467:63–70. https://doi.org/10.1016/j.aquaculture.2016.06.038
MontanhiniNeto R, Ostrensky A (2015) Evaluation of commercial feeds intended for the Brazil production of Nile tilapia (Oreochromis niloticus L.): nutritional and environmental implications. Aquac Nutr 21:311–320. https://doi.org/10.1111/anu.12154
Montoya‐Camacho N, Marquez‐Ríos E, Castillo‐Yáñez FJ, López JLC, López‐Elías JA, Ruíz‐Cruz S, Jiménez‐Ruíz EI, Rivas‐Veja ME, Ocaño‐Higuera VM (2018) Advances in the use of alternative protein sources for tilapia feeding. Rev Aquac 11:515–526. https://onlinelibrary.wiley.com/doi/abs/10.1111/raq.12243
Nascimento HS, Crispim BA, Francisco LFV, Merey FM, Kummrow F, Viana LF, Inoue LAKA, Barufatti A (2020) Genotoxicity evaluation of three anesthetics commonly employed in aquaculture using Oreochromis niloticus and Astyanax lacustris. Aquac Rep 17:100357. https://doi.org/10.1016/j.aqrep.2020.100357
Nguyen L, Kubitza F, Salem SMR, Hanson TR, Davis DA (2019) Comparison of organic and inorganic microminerals in all plant diets for Nile tilapia Oreochromis niloticus. Aquaculture 498:297–304. https://doi.org/10.1016/j.aquaculture.2018.08.034
NRC (2011) Nutrient requirements of fish and shrimp. The National Academy Press, Washington
Ogino C, Yang GY (1978) Requirement of rainbow trout for dietary zinc. Bull Japan Soc Sci Fish 44:1015–1018. https://doi.org/10.2331/suisan.44.1015
Pietsch C (2020) Risk assessment for mycotoxin contamination in fish feeds in Europe. Mycotoxin Res 36:41–62. https://doi.org/10.1007/s12550-019-00368-6
Pinheiro-Sousa DB, Torres Junior AR, Silva D, Santos RL, CarvalhoNeta RNF (2019) A screening test based on hematological and histological biomarkers to evaluate the environmental impacts in tambaqui (Colossoma macropomum) from a protected area in Maranhão, Brazilian Amazon. Chemosphere 214:445–451. https://doi.org/10.1016/j.chemosphere.2018.09.146
Prabhu PAJ, Schrama JW, Kaushik SJ (2016) Mineral requirements of fish: a systematic review. Rev Aquac 8:172–219. https://doi.org/10.1111/raq.12090
Prabhu PAJ, Schrama JW, Fontagné-Dicharry S, Mariojouls C, Surget A, Bueno M, Geurden I, Kaushik SJ (2018) Evaluating dietary supply of microminerals as a premix in a complete plant ingredient-based diet to juvenile rainbow trout (Oncorhynchus mykiss). Aquac Nutr 24:539–547. https://doi.org/10.1111/anu.12586
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Samuelsen TA, Oterhals Å (2016) Water-soluble protein level in fishmeal affects extrusion behaviour, phase transitions and physical quality of feed. Aquac Nutr 22:120–133. https://doi.org/10.1111/anu.12235
Sarker PK, Fournier J, Boucher E, Proulx E, Noüe J, Vandenberg GW (2011) Effects of low phosphorus ingredient combinations on weight gain, apparent digestibility coefficients, non-fecal phosphorus excretion, phosphorus retention and loading of large rainbow trout (Oncorhynchus mykiss). An Feed Sci Techn 168:241–249. https://doi.org/10.1016/j.anifeedsci.2011.04.086
Schamber CR, Boscolo WR, Natali MRM, Michelato M, Furuya VRB, Furuya WM (2014) Growth performance and bone mineralization of large Nile tilapia (Oreochromis niloticus) fed graded levels of available phosphorus. Aquac Int 22:1711–1721. https://doi.org/10.1007/s10499-014-9776-4
Séité S, Mourier A, Camougrand N, Salin B, Figueiredo-Silva AC, Fontagné-Dicharry S, Panserat S, Seiliez I (2018) Dietary methionine deficiency affects oxidative status, mitochondrial integrity and mitophagy in the liver of rainbow trout (Oncorhynchus mykiss). Sci Rep 8:10151. https://doi.org/10.1038/s41598-018-28559-8
Song Y, Leonard SW, Traber MG, Ho E (2009) Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J Nutr 139(9):1626–1631. https://doi.org/10.3945/jn.109.106369
Sørensen S (2012) A review of the effects of ingredient composition and processing conditions on the physical qualities of extruded high-energy fish feed as measured by prevailing methods. Aquac Nutr 18:233–248. https://doi.org/10.1111/j.1365-2095.2011.00924.x
Stankevičiūtė M, Butrimavičienė L, Valskienė R, Greiciūnaitė J, Baršienė J, Vosylienė MZ, Svecevičius G (2016) Analysis of nuclear abnormalities in erythrocytes of rainbow trout (Oncorhynchus mykiss) treated with Cu and Zn and after 4-, 8-, and 12-day depuration (post-treatment recovery). Mut Res 797:26–35. https://doi.org/10.1016/j.mrgentox.2016.01.003
Stevens JR, Newton RW, Tlusty M, Little DC (2018) The rise of aquaculture by-products: increasing food production, value, and sustainability through strategic utilization. Mar Policy 90:115–124. https://doi.org/10.1016/j.marpol.2017.12.027
Tacon AGJ, Metian M (2008) Aquaculture feed and food safety: the role of the food and agriculture organization and the Codex Alimentarius. Ann N Y Acad Sci 1140:50–59. https://doi.org/10.1196/annals.1454.003
Tacon AGJ, Lemos D, Metian M (2020) Fish for health: improved nutritional quality of cultured fish for human consumption. Rev Fish Sci Aquac 28(4):449–458. https://doi.org/10.1080/23308249.2020.1762163
Tavares-Dias M, Moraes FR (2003) Características hematológicas de Tilapia rendalli Boulenger, 1896 (Osteichthyes: Cichlidae) capturada em “pesque-pague” de França, São Paulo, Brasil. Biosci J 19:107–114. http://www.seer.ufu.br/index.php/biosciencejournal/article/view/6443
Teodósio R, Engrola S, Colen R, Masagounder K, Aragão C (2019) Optimizing diets to decrease environmental impact of Nile tilapia (Oreochromis niloticus) production. Aquac Nutr 1–10https://doi.org/10.1111/anu.13004
Thomas M, van Zuilichem DJ, van der Poel AFB (1997) Physical quality of pelleted animal feed. 2. contribution of processes and its conditions. An Feed Sci Techn 64:173–192. https://doi.org/10.1016/S0377-8401(96)01058-9
Tran-Ngoc KT, Haidar MN, Roem AJ, Sendão J, Verreth JAJ, Schrama JW (2019) Effects of feed ingredients on nutrient digestibility, nitrogen/energy balance and morphology changes in the intestine of Nile tilapia (Oreochromis niloticus). Aquac Res 50:2577–2590. https://doi.org/10.1111/are.14214
Wang X, Fenech M (2003) A comparison of folic acid and 5-methyltetrahydrofolate for prevention of DNA damage and cell death in human lymphocytes in vitro. Mutagenesis 18:81–86. https://doi.org/10.1093/mutage/18.1.81
Wei T, Simko V (2016) R package 'corrplot': visualization of a correlation matrix. (Version 0.88), https://github.com/taiyun/corrplot. Accessed 28 May 2019
Yao YF, Jiang M, Wen H, Wu F, Liu W, Tian J, Yang CG (2014) Dietary phosphorus requirement of GIFT strain of Nile tilapia Oreochromis niloticus reared in freshwater. Aquac Nutr 20:273–280. https://doi.org/10.1111/anu.12075
Yuan Y, Yuan Y, Dai Y, Gong Y (2017) Economic profitability of tilapia farming in China. Aquacult Int 25:1253–1264. https://doi.org/10.1007/s10499-017-0111-8
Zaminhan M, Boscolo WR, Neu DH, Feiden A, Furuya VRB, Furuya WM (2017) Dietary tryptophan requirements of juvenile Nile tilapia fed corn-soybean meal-based diets. Animal Feed Sci Technol 227:62–67. https://doi.org/10.1016/j.anifeedsci.2017.03.010
Zhang Z, Bi M, Yang J, Yao H, Liu Z, Xu S (2017) Effect of phosphorus deficiency on erythrocytic morphology and function in cows. J Vet Sci 18(3):333–340. https://doi.org/10.4142/jvs.2017.18.3.333
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This study was partially funded by CAPES — Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (Funding Code 001), CNPq — Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant numbers 421884/2016–9, 311975/2018–6 CALC), FUNDECT — Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (grant number 59/300.222/2016), FINEP — Financiadora de Inovação e Pesquisas, and PIBAP — Programa Institucional de Bolsas aos Alunos de Pós-Graduação da Universidade Estadual de Mato Grosso do Sul.
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Erika do Carmo Ota: research design, data collection, literature review, data analysis, statistical analysis, and article writing. Claudia Andrea Lima Cardoso: research design, project administration, and article writing. Luis Antonio Kioshi Aoki Inoue: research design, data collection, and article writing. Ricardo Basso Zanon: data collection and article writing. Tarcila Souza de Castro Silva: research design, funding acquisition, project administration, data collection, data analysis, and article writing.
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Ota, E.d.C., Cardoso, C.A.L., Inoue, L.A.K.A. et al. Fish feed can show genotoxic damage. Fish Physiol Biochem 48, 735–748 (2022). https://doi.org/10.1007/s10695-022-01068-2
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DOI: https://doi.org/10.1007/s10695-022-01068-2